N(6)-methyladenosine-binding protein YTHDF1 suppresses EBV replication and promotes EBV RNA decay

EMBO Rep. 2021 Apr 7;22(4):e50128. doi: 10.15252/embr.202050128. Epub 2021 Feb 19.

Abstract

N6 -methyladenosine (m6 A) modification of mRNA mediates diverse cellular and viral functions. Infection with Epstein-Barr virus (EBV) is causally associated with nasopharyngeal carcinoma (NPC), 10% of gastric carcinoma, and various B-cell lymphomas, in which the viral latent and lytic phases both play vital roles. Here, we show that EBV transcripts exhibit differential m6 A modification in human NPC biopsies, patient-derived xenograft tissues, and cells at different EBV infection stages. m6 A-modified EBV transcripts are recognized and destabilized by the YTHDF1 protein, which leads to the m6 A-dependent suppression of EBV infection and replication. Mechanistically, YTHDF1 hastens viral RNA decapping and mediates RNA decay by recruiting RNA degradation complexes, including ZAP, DDX17, and DCP2, thereby post-transcriptionally downregulating the expression of EBV genes. Taken together, our results reveal the critical roles of m6 A modifications and their reader YTHDF1 in EBV replication. These findings contribute novel targets for the treatment of EBV-associated cancers.

Keywords: Epstein-Barr virus; RNA decay; YTHDF1; m6A modification; viral replication.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / analogs & derivatives
  • Carrier Proteins
  • Epstein-Barr Virus Infections*
  • Herpesvirus 4, Human / genetics
  • Humans
  • Nasopharyngeal Neoplasms*
  • RNA Stability
  • RNA-Binding Proteins / genetics
  • Virus Replication

Substances

  • Carrier Proteins
  • RNA-Binding Proteins
  • YTHDF1 protein, human
  • N-methyladenosine
  • Adenosine